Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 110(3): 319-323, May 2015 319

The rising importance of Triatoma rubrofasciata

Jean-Pierre Dujardin1/+, Truong Xuan Lam2, Pham Thi Khoa3, Christopher John Schofield4

1Unité Mixte de Recherche 177-Interactions Hôte-Vecteur-Parasite-Enrironnement dans les Maladies Tropicales Négligées dues aux Trypanosomatidés, Centre International de Recherches Agronomiques pour le Développement, Institut de Recherches pour le Développement, Campus international de Baillarguet, Montpellier, France 2Institute of Ecology and Biological Resources, Vietnam Academy of Sciences and Technology, Hanoi, Vietnam 3National Institute of Malariology, Parasitology and Entomology, Hanoi, Vietnam 4London School of Tropical Medicine and Hygiene, London, UK

The migration of invasive vector species has contributed to the worldwide extension of infectious diseases such as dengue (Aedes aegypti) and chikungunya (Aedes albopictus). It is probably a similar behaviour for certain vec- tors of Chagas disease which allowed it to become a continental burden in Latin America. One of them, Triatoma rubrofasciata has also been spreading throughout the tropical and subtropical world. Here, the recent and massive peridomestic presence of T. rubrofasciata in Vietnam cities is reported, and tentatively explained, highlighting the need for improved entomological surveillance.

Key words: Vietnam - Triatoma rubrofasciata - sp.

In the XVIII century, Bernardin de Saint-Pierre de- bugs able to survive in other tropical and subtropical scribed, at the island of La Reunion, a kind of punaise countries or of uninfected bugs that could become estab- des bois (“sylvatic stinkbug”) by these words: “... its bite lished and then catch the parasite from a Latin immigrant is more dangerous than the scorpion; it is followed by a (Schofield et al. 2009). At present, the risk for such a sce- tumour the size of a pigeon’s egg, which dissipates after nario seems to be low, but it is supported by the situation five or six days” [translated from Mar­tin (1820)]. Three recently denounced in Vietnam, where T. rubrofasciata centuries later, we received from the same La Reunion develops a propensity to feed on humans. This short note island a few pictures of a bug “found in the bed of a presents some statistics about the peridomestic infestation child”, a bug we identified as Triatoma rubrofasciata by T. rubrofasciata in Vietnam and discusses the possible (: ). This simple story sent us a scenarios underlying this relatively recent phenomenon. kind of warning because, after three centuries, the bug T. rubrofasciata in Vietnam - Although recorded in was no more a punaise des bois, it had come to be a bug Vietnam since Kalshoven (1970) and recently confirmed “found in the bed of a child”. in Vietnam by national entomologists (Truong 2004), it The domestic habits of some haematophagous Hemi- is only a few years ago that the tropicopolitan T. rubro- ptera of the subfamily represent the main fasciata became a cause of concern for health authori- risk for humans to be infected by - ties. In the last decade, many people made complaints of causative agent of Chagas disease. Since these being attacked by an “assassin” bug in different places of are found predominantly in the New World, particularly Vietnam - mainly Hanoi and other large cities - leading in Latin America, Chagas disease is an endemic disease local health authorities to seek national and international typically considered as limited to the American conti- entomological expertise. The incriminated bug was T. nent. However, a number of people infected by T. cruzi rubrofasciata. A national survey between 2010-2012 acquired the infection in the Old World through blood confirmed that it could be found in at least 21 provinces transfusion from Latin immigrants unaware of their own of Vietnam, with a seasonal peak of adult bugs found infection [eg., Gascon et al. (2010)]. Since the parasite can from June-September. Heavy infestations, involving be transmitted by blood transfusion and organ transplant, hundreds of insects per house, were reported both from the increasing transcontinental exchanges mean that urban and rural areas, with the highest densities found Chagas disease is no longer restricted to the American in urban areas (Truong & Dujardin 2013, Van Chau et al. continent (Coura & Viñas 2010, Tanowitz et al. 2011). 2013). Major cities were particularly affected, especially Migration of the vectors might also help to Hanoi (Fig. 1) which is located at more than 100 km from spread the disease beyond its previous limits. This could the coast at Hai Phong. The common micro-habitat was occur through the accidental transportation of infected found close to human dwellings where wood, firewood or waste were accumulated. In the Long Bien and Tu Liem districts of Hanoi, T. rubrofasciata populations were concentrated in large peridomestic shelters with all de- velopment stages (eggs, nymphs and adults) readily ob- served. In general, these shelters were also infested with doi: 10.1590/0074-02760140446 Financial support: IRD, NAFOSTED (106.15-2010.24) rats, but the bugs were also found in association with + Corresponding author: [email protected] chickens (Truong & Dujardin 2013). In big cities such Received 26 November 2014 as Hanoi, Danang and Ho Chi Minh, adult specimens Accepted 3 February 2015 of T. rubrofasciata were also reported in buildings from

online | memorias.ioc.fiocruz.br 320 T. rubrofasciata in Asia • Jean-Pierre Dujardin et al.

Fig. 1: map of Hanoi Province. Red dots correspond to sites positive for Triatoma rubrofasciata (Truong & Dujardin 2013).

TABLE I Asiatic Triatominae

Africa: Angola, Congo (Katanga), Guinea (Conakry), Saudi Arabia, Sierra Leone, South Africa, Tanzania Atlantic Ocean: Azores Asia -Pacific: Andaman Islands, Burma (Myanmar), Cambodia, Carolina Islands, China, Comoros Islands, India, Indonesia, Japan, Madagascar, Mauritius, Philippines, Reunion, Rodriguez Islands, Sri Lanka, Singapore, Seychelles, Taiwan, Thailand, Tonga, Vietnam Americas: Argentina (Buenos Aires), Brazil (Atlantic coastal areas), Cuba (and most other Caribbean Triatoma rubrofasciata islands), French Guiana, Suriname, Venezuela, United States of America (Florida, Hawaii)

Triatoma amicitiae Sri Lanka Triatoma bouvieri Philippines, Vietnam Triatoma cavernicola Malaysia Triatoma leopoldi Australia (North Queensland), Indonesia Triatoma pugasi Indonesia (Java) Triatoma migrans India, Indonesia, Malaysia, Philippines, Thailand Triatoma sinica China Linshcosteus sp. India the reported geographical distribution of T. rubrofasciata and other Old World Triatominae [updated from Ryckman and Archbold (1981) and Schofield et al. (2009)]. Note that many of the records are old (pre-1945) and may not reflect current distribution.

the ground floor up to the eighth floor, biting sleeping conorhini worldwide. Excluding infections in Latin people and hiding in their beds. American migrants, T. cruzi is found exclusively in the Rural infestations were apparently less dense, but ge- New World and is infective to humans and most other ographically extended deep into the continent. The peri- mammals. By contrast, T. conorhini was first recorded domestic presence of T. rubrofasciata was also reported to in the intestine of T. rubrofasciata in Madras, in 1909, the northeast of Hanoi, extending across the frontier well and subsequently reported from T. rubrofasciata in many into southern China (W Cai, unpublished observations). other locations around the world, including Latin Ameri- T. rubrofasciata is known to transmit at least two ca (Miles 2013). A T. conorhini-like trypanosome, indis- parasites: T. cruzi in Latin America and Trypanosoma tinguishable from T. conorhini by random amplification Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 110(3), May 2015 321

Outside the American continent, there are a few other species classified as belonging to the Triatoma, called the “Asiatic Triatoma”, as well as a few species of another genus, the morphologically distinct Linshcosteus genus (Table I). Except for T. rubrofasciata, the Triatoma species described today in Asia do not occur in the New World and vice versa. Two hypotheses competed during decades, one defending an Asian origin for this species, the other suggesting an American origin (Table II). The hypothesis which is retained today is that T. rubrofasciata, because of its close association with do- mestic rats (especially R. rattus), has been transported Fig. 2: local skin reaction to the bite of Triatoma rubrofasciata (photo on ships along early international trade routes during by one the authors, TXL). the XVI to XIX centuries (Schofield 1988, Gorla et al. 1997, Patterson et al. 2001). In this hypothesis of a New World origin however, more knowledge is needed to of polymorphic DNA was discovered recently in another fully understand the distribution of both T. cruzi and T. species of triatomine bug, Linshcosteus karupus in India conorhini (Table II). More data are also needed on T. (Miles 2013). In the recent surveys in Vietnam, trypano- rubrofasciata, since wild foci that might represent the somatid forms have been recognised in the intestine of original populations have never been reported. the bugs at a high frequency (50-90%); the parasite is not In the hypothesis of T. rubrofasciata being an in- definitively identified, although its general morphology troduced species to Vietnam, the situation would cor- indicates a Megatrypanum species such as T. conorhini. respond to the one already described in the New World, The natural host of T. conorhini was discovered in 1937 where domestic populations are frequently “exported” in Java: rats of the species Rattus rattus L. (the ship rat) populations, i.e., bugs introduced with humans by pas- were shown to be infected by feeding uninfected bugs on sive transportation. As an insect introduced by humans them (xenodiagnosis). Rats were also shown to eat infected outside its previous limits, T. rubrofasciata stayed with bugs when given the opportunity and to become infected. humans and adapted more and more to them. Laboratory experiments on mice suggest that the natural The known domestic hosts of T. rubrofasciata are the route of the rat infection is by contamination with bug fae- rat - probably Rattus exulans and Rattus norvegicus in Vietnam (Morand 2013) - and the hen (Sherwin & Wood ces and not by the bite of the infected bug (Miles 2013). 1946). These two hosts support two different assumptions It is not known if humans have ever been infected regarding its origins. The ship rat is the host that suits the with T. conorhini. So far in Vietnam, no trypanosome idea of migration by sea, as it is readily found in the ves- parasite has been detected in Giemsa-stained blood sels carrying food, especially in past centuries where hy- smears from blood taken seven-10 days after being bit- giene was less strict. Chickens however are the hosts that ten by T. rubrofasciata (Van Chau et al. 2013), but con- best fit the hypothesis of domestication. They are readily tamination of food with triatomine bug faeces might oc- fed upon by most kissing bugs. In the rural areas of Latin cur, leading to exposure to infection by the oral route. America, they often appear as an important intermediate Another epidemiological consideration is the spread of in the bugs’ transition from silvatic to domestic ecotopes. human immunodeficiency virus infection, which might Thinking of long voyages, one might imagine that for T. lead to the occurrence of T. conorhini infections in im- rubrofasciata the gate of “Departures” is the rat and the munocompromised patients (Miles 2013). gate of “Arrivals” is the hen house (Dujardin 2013). Today, T. rubrofasciata in Vietnam is a serious nui- Whatever the hypothesis about T. rubrofasciata origins, sance. People bitten by the bug (mostly on legs and arms) the recent character of its massive and widespread infesta- presented swelling and itching at the bite (Fig. 2), some- tion in Vietnam is unclear. An external trigger event could times with consecutive local skin infection. In Hanoi, have been the fight against avian influenza. In the previ- 24% of cases also involved severe fever lasting one-two ous decade, campaigns against avian influenza (mainly days (Truong & Dujardin 2013), although for the whole H5N1) in Vietnam led to large-scale slaughter of perido- of Vietnam the average fever rate following a bite was mestic chickens - especially in urban and periurban areas. around 5% (Van Chau et al. 2013). Repeated exposure So it may be that this sudden loss of a primary host for the to triatomine bites or to triatomine faeces may cause peridomestic T. rubrofasciata populations, triggered a host immunological reactions (Walter et al. 2012) and some- switch to available humans (Schofield et al. 2014). times severe anaphylaxis that can be fatal (Teo & Cheah T. rubrofasciata is an invasive species which, despite its 1973, Lo Vecchio & Tran 2004, Wang & Peng 2006). large size and its irritating saliva, seems to be increasing its The origins of T. rubrofasciata in Vietnam - Discus- association with humans. In Vietnam it is already a matter sion of the origins of T. rubrofasciata in Vietnam, or else- of concern because of its bites and the bite reaction that can where in the Old World, involves discussing the whole ge- ensue. With increased migration of human populations and ographic distribution of Triatominae. The vast majority of further development of anthropophilia of T. rubrofasciata, species (95%) is limited to the New World, which suggests it seems entirely possible that T. cruzi infections reaching an American origin for the members of this subfamily. Asia could be picked up by urban T. rubrofasciata. 322 T. rubrofasciata in Asia • Jean-Pierre Dujardin et al.

TABLE II The possible origin of Triatoma rubrofasciata

An Asian origin for T. rubrofasciata An American origin for T. rubrofasciata

Parasite argument Ryckman and Archbold (1981) noted that although T. rubrofasciata The probability of being infected by T. cruzi a few centuries is the host of Trypanosoma cruzi and Trypanosoma conorhini in ago was not necessarily the same as today. The geographi- the New World, it had never met with T. cruzi in the Old World. cal expansion of T. cruzi to domestic (like Rattus This argument convinced them that T. rubrofasciata arrived in the rattus) in the Americas was the result of massive migra- New World with its natural parasite, T. conorhini, and was second- tion of domestic vectors like , Rhodnius arily infected by T. cruzi. prolixus or , that occurred only very re- cently (Schofield 1988, Dujardin 1998). It has been suggested that the Asian monkey Macaca was the natural It is not unlikely that the Macaca reared in a South Ameri- host of T. conorhini (Deane et al. 1986, Miles 2013). can laboratory could have been infected during their trans- portation to other continents.

Insect argument There are other Triatoma species in Asia, not only rubrofasciata T. rubrofasciata would be the common ancestor of the other (Table I). Asiatic species, including Linshcosteus (Hypsa et al. 2002). The first collections of T. rubrofasciata were Asian. In fact, the Morphometric and molecular studies (Gorla et al. 1997, Pat- species described by De Geer 1773 was collected aux Indes (be- terson et al. 2001, Hypsa et al. 2002, Hwang & Weirauch lieved to indicate the then Dutch East Indies or Indonesia). It rep- 2012) suggest a New World origin for the “Asiatic clade” resents the type species of the genus Triatoma. of Triatominae.

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